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Ecological Immunology of mosquito-malaria interactions: Of non-natural versus natural model systems and their inferences

Published online by Cambridge University Press:  02 June 2009

F. TRIPET
F. TRIPET*
Affiliation:
Center for Applied Entomology and Parasitology, School of Life Sciences – Huxley Building, Keele University Campus, Keele, StaffordshireST5 5BG, UK
*
*Corresponding Author: Frederic Tripet, Center for Applied Entomology and Parasitology, School of Life Sciences, Huxley Building, Keele University Campus, Keele, Staffordshire ST5 5BGUK. Tel: ++44 1782 733873; Fax: ++44 1782 733516; Email: tripet@biol.keele.ac.uk
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Summary

There has been a recent shift in the literature on mosquito/Plasmodium interactions with an increasingly large number of theoretical and experimental studies focusing on their population biology and evolutionary processes. Ecological immunology of mosquito-malaria interactions – the study of the mechanisms and function of mosquito immune responses to Plasmodium in their ecological and evolutionary context – is particularly important for our understanding of malaria transmission and how to control it. Indeed, describing the processes that create and maintain variation in mosquito immune responses and parasite virulence in natural populations may be as important to this endeavor as describing the immune responses themselves. For historical reasons, Ecological Immunology still largely relies on studies based on non-natural model systems. There are many reasons why current research should favour studies conducted closer to the field and more realistic experimental systems whenever possible. As a result, a number of researchers have raised concerns over the use of artificial host-parasite associations to generate inferences about population-level processes. Here I discuss and review several lines of evidence that, I believe, best illustrate and summarize the limitations of inferences generated using non-natural model systems.

Keywords

Anopheles gambiaePlasmodium falciparummosquito-malaria interactionsmodel systemsinferencesecological immunologymicro-coevolutionmacro-coevolution life history trade-offstranscriptomes
Type
Research Article
Information
Parasitology , Volume 136 , Special Issue 14: Transmission cycles in protozoan parasites , December 2009 , pp. 1935 - 1942
Copyright
Copyright © Cambridge University Press 2009

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References

REFERENCES

Andersson, M. (1986). Evolution of condition-dependent sex ornaments and mating preferences – sexual selection based on viability differences. Evolution 40, 804–816.CrossRefGoogle ScholarPubMed
Boete, C. (2005). Malaria parasites in mosquitoes: laboratory models, evolutionary temptation and the real world. Trends in Parasitology 21, 445–447.Google Scholar
Cohuet, A., Osta, M. A., Morlais, I., Awono-Ambene, P. H., Michel, K., Simard, F., Christophides, G. K., Fontenille, D. and Kafatos, F. C. (2006). Anopheles and Plasmodium: from laboratory models to natural systems in the field. EMBO Report 7, 1285–1289.CrossRefGoogle ScholarPubMed
Dawkins, R. (1976). The Selfish Gene, Oxford, Oxford University Press.Google Scholar
Deerenberg, C., Arpanius, V., Daan, S. and Bos, N. (1997). Reproductive effort decreases antibody responsiveness. Proceedings of the Royal Society of London B 264, 1021–1029.CrossRefGoogle Scholar
Dong, Y., Aguilar, R., Xi, Z., Warr, E., Mongin, E. and Dimopoulos, G. (2006). Anopheles gambiae immune responses to human and rodent Plasmodium parasite species. PLoS Pathogens 2, e52.Google Scholar
Ebert, D. (1994). Virulence and local adaptation of a horizontally transmitted parasite. Science 265, 1084–1086.CrossRefGoogle ScholarPubMed
Ebert, D. and Herre, E. A. (1996). The evolution of parasitic diseases. Parasitology Today 12, 96–101.CrossRefGoogle ScholarPubMed
Escalante, A. A. and Ayala, F. J. (1994). Phylogeny of the malarial genus Plasmodium, derived from ribosomal-RNA gene-sequences. Proceedings of the National Academy of Sciences, USA 91, 11373–11377.Google Scholar
Escalante, A. A. and Ayala, F. J. (1995). Evolutionary origin of Plasmodium and other Apicomplexa based on ribosomal-RNA genes. Proceedings of the National Academy of Sciences, USA 92, 5793–5797.CrossRefGoogle Scholar
Ewald, P. W. (1983). Host-parasite relations, vectors, and the evolution of disease severity. Annual Review Ecology and Systematics 14, 465–485.CrossRefGoogle Scholar
Ferguson, H. M. and Read, A. F. (2002). Why is the effect of malaria parasites on mosquito survival still unresolved? Trends in Parasitology 18, 256–261.Google Scholar
Folstad, I. and Karter, A. J. (1992). Parasites, bright males and the immunocompetence handicap. American Naturalist 139, 603–622.CrossRefGoogle Scholar
Forbes, M. R. L. (1993). Parasitism and host reproductive effort. OIKOS 67, 444–450.CrossRefGoogle Scholar
Gandon, S., Capowiez, Y., Dubois, Y., Michalakis, Y. and Olivieri, I. (1996). Local adaptation and gene-for-gene coevolution in a metapopulation model. Proceedings of the Royal Society of London B 263, 1003–1009.Google Scholar
Gandon, S. and Michalakis, Y. (2002). Local adaptation, evolutionary potential and host-parasite coevolution: interactions between migration, mutation, population size and generation time. Journal of Evolutionary Biology 15, 451–462.CrossRefGoogle Scholar
Garnham, P. C. (1963). Malaria Parasites and Other Haemosporida, Blackwell Scientific Publications, Oxford.Google Scholar
Greischar, M. A. and Koskella, B. (2007). A synthesis of experimental work on parasite local adaptation. Ecology Letters 10, 418–434.CrossRefGoogle ScholarPubMed
Hamilton, W. D. (1964 a). The genetical evolution of social behavior. II. Journal of Theoretical Biology 7, 17–52.CrossRefGoogle Scholar
Hamilton, W. D. (1964 b). The genetical evolution of social behaviour. I. Journal of Theoretical Biology 7, 1–16.CrossRefGoogle ScholarPubMed
Hamilton, W. D. and Zuk, M. (1982). Heritable true fitness and bright birds: a role for parasites? Science 218, 384–387.CrossRefGoogle Scholar
Huff, C. G. (1927). Studies on the infectivity of Plasmodia of birds for mosquitoes with special reference to the problem of immunity in the mosquito. American Journal of Tropical Medicine and Hygiene 7, 706–734.Google Scholar
Huff, C. G. (1935). Natural immunity and susceptibility of culicine mosquitoes to avian malaria. American Journal of Tropical Medicine and Hygiene 15, 427–434.CrossRefGoogle Scholar
Hume, J. C. C., Tunnicliff, M., Ranford-Cartwright, L. C. and Day, K. P. (2007). Susceptibility of Anopheles gambiae and Anopheles stephensi to tropical isolates of Plasmodium falciparum. Malaria Journal 6, 139. doi: 10.1186/1475-2875-6-139.CrossRefGoogle ScholarPubMed
Joy, D. A., Gonzalez-Ceron, L., Carlton, J. M., Gueye, A., Fay, M., Mccutchan, T. F. and Su, X. Z. (2008). Local adaptation and vector-mediated population structure in Plasmodium vivax malaria. Molecular Biology and Evolution 25, 1245–1252.CrossRefGoogle ScholarPubMed
Killick-Kendrick, R. and Peters, W. (1978). Rodent Malaria. Academic Press, London, New York, San Francisco.Google Scholar
Konig, C. and Schmid-Hempel, P. (1995). Foraging activity and immunocompetence in workers of the bumble bee, Bombus terrestris L. Proceedings of the Royal Society of London B 260, 225–227.Google Scholar
Kraaijeveld, A. R. and Godfray, H. C. (1997). Trade-off between parasitoid resistance and larval competitive ability in Drosophila melanogaster. Nature 389, 278–280.CrossRefGoogle ScholarPubMed
Kurtz, J. (2000). Gender differences and individual variation in the immune system of the scorpionfly Panorpa vulgaris (Insecta: Mecoptera). Developmental and Comparative Immunology 24, 1–12.CrossRefGoogle ScholarPubMed
Lochmiller, R. L., Vestey, M. R. and Boren, J. C. (1993). Relationship between protein nutritional-status and immunocompetence in northern bobwhite chicks. Auk 110, 503–510.CrossRefGoogle Scholar
Martinsen, E. S., Perkins, S. L. and Schall, J. J. (2008). A three-genome phylogeny of malaria parasites (Plasmodium and closely related genera): evolution of life-history traits and host switches. Molecular Phylogenetics and Evolution 47, 261–273.CrossRefGoogle ScholarPubMed
May, R. M. and Anderson, R. M. (1983). Epidemiology and genetics in the coevolution of parasites and hosts. Proceedings of the Royal Society of London B 219, 281–313.Google ScholarPubMed
Mendes, A. M., Schlegelmilch, T., Cohuet, A., Awono-Ambene, P., De Iorio, M., Fontenille, D., Morlais, I., Christophides, G. K., Kafatos, F. C. and Vlachou, D. (2008). Conserved mosquito/parasite interactions affect development of Plasmodium falciparum in Africa. PLoS Pathogens 4, e1000069.CrossRefGoogle ScholarPubMed
Michel, K., Suwanchaichinda, C., Morlais, I., Lambrechts, L., Cohuet, A., Awono-Ambene, P. H., Simard, F., Fontenille, D., Kanost, M. R. and Kafatos, F. C. (2006). Increased melanizing activity in Anopheles gambiae does not affect development of Plasmodium falciparum. Proceedings of the National Academy of Science, USA 103, 16858–16863.CrossRefGoogle Scholar
Moller, A. P. and Saino, N. (1994). Parasites, immunology of hosts, and host sexual selection. Journal of Parasitology 80, 850–858.CrossRefGoogle ScholarPubMed
Perkins, S. L., Sarkar, I. N. and Carter, R. (2007). The phylogeny of rodent malaria parasites: simultaneous analysis across three genomes. Infection Genetics and Evololution 7, 74–83.CrossRefGoogle ScholarPubMed
Perrin, N., Christe, P. and Richner, H. (1996). On host life-history response to parasitism. Oikos 79, 317–320.Google Scholar
Poulin, R. (2007). Evolutionary Ecology of Parasites. 2nd Edn.Princeton University Press.CrossRefGoogle Scholar
Poulin, R., Morand, S. and Skorping, A. (2000). Evolutionary Biology of Host-Parasite Relationships: Theory Meets Reality. Elsevier Health Sciences.Google Scholar
Price, P. W. (1980). Evolutionary Biology of Parasites, Princeton University Press.Google ScholarPubMed
Price, P. W. (1984). Chapter 6: Parasite and host interactions. In Insect Ecology, 2nd Edn.John Wiley & Sons, New York.Google Scholar
Prugnolle, F., De Meeus, T., Pointier, J. P., Durand, P., Rognon, A. and Theron, A. (2006). Geographical variations in infectivity and susceptibility in the host-parasite system Schistosoma mansoni/Biomphalaria glabrata: no evidence for local adaptation. Parasitology 133, 313–319.CrossRefGoogle ScholarPubMed
Richner, H. and Tripet, F. (1999). Ectoparasitism and the trade-off between current and future reproduction. Oikos 86, 535–538.CrossRefGoogle Scholar
Rolff, J. and Siva-Jothy, M. T. (2003). Invertebrate ecological immunology. Science 301, 472–475.CrossRefGoogle ScholarPubMed
Roy, S. W. and Irimia, M. (2008). Origins of human malaria: rare genomic changes and full mitochondrial genomes confirm the relationship of Plasmodium falciparum to other mammalian parasites but complicate the origins of Plasmodium vivax. Molecular Biology and Evolution 25, 1192–1198.Google Scholar
Schmid-Hempel, R. and Schmid-Hempel, P. (1998). Colony performance and immunocompetence of a social insect,Bombus terrestris, in poor and variable environments. Functional Ecology 12, 22–30.CrossRefGoogle Scholar
Sheldon, B. C. and Verhulst, S. (1996). Ecological immunology: costly parasite defences and trade-offs in evolutionary ecology. Trends in Ecology and Evolution 11, 317–321.CrossRefGoogle ScholarPubMed
Siva-Jothy, M. T., Tsubaki, Y. and Hooper, R. (1998). Decreased immune response as a proximate cost of copulation and oviposition in a damselfly. Physiological Entomology 23, 274–277.CrossRefGoogle Scholar
Tripet, F., Aboagye-Antwi, F. and Hurd, H. (2008). New horizons: ecological immunology of mosquito-malaria interactions. Trends in Parasitology 24, 219–227.CrossRefGoogle Scholar
Waters, A. P., Higgins, D. G. and McCutchan, T. F. (1991). Plasmodium falciparum appears to have arisen as a result of lateral transfer between avian and human hosts. Proceedings of the National Academy of Science USA 88, 3140–3144.Google Scholar
Waters, A. P., Higgins, D. G. and McCutchan, T. F. (1993). Evolutionary relatedness of some primate models of Plasmodium. Molecular Biology and Evolution 10, 914–923.Google Scholar
Yoeli, M., Vanderberg, J., Nawrot, R. and Most, H. (1965). Studies on sporozoite-induced infections of rodent malaria II. Anopheles stephensi as an experimental vector for Plasmodium Berghei. American Journal of Tropical Medicine and Hygiene 14, 927–930.Google Scholar